Temporomandibular joint problems in patients with rheumatoid arthritis

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Temporomandibular joint disorders in patients with rheumatoid arthritis

Teresa Sadura-Sieklucka¹ÎD, Jakub Gębicki², Beata Sokołowska³ÎD, Przemysław Markowski⁴, Beata Tarnacka²ÎD

1Department of Geriatrics, National Institute of Geriatrics, Rheumatology and Rehabilitation, Warsaw, Poland

2Department of Rehabilitation, Faculty of Medicine, Medical University of Warsaw, Poland

3Bioinformatics Laboratory, Mossakowski Medical Research Centre, Polish Academy of Sciences, Warsaw, Poland

4Clinic of Rehabilitation, National Institute of Geriatrics, Rheumatology and Rehabilitation, Warsaw, Poland

Abstract

Objectives: The aim of this study is to draw the attention of patients, doctors and therapists to the importance of temporomandibular joint (TMJ) problems in rheumatoid arthritis (RA).

Material and methods: The research was conducted at the National Institute of Geriatrics Rheu

matology and Rehabilitation in Warsaw. The study involved 60 subjects. The test group consists of 30 patients with diagnosed RA. The control group (n = 30) consisted of healthy participants of simi

lar age. The study analyzed the occurrence of problems in TMJ joints, acoustic phenomena and the level of pain. Masseter muscle development, range of abduction motion and pain during palpation of soft tissues were assessed on the basis of the joint pain map of Prof. Mariano Rocabado.

Results: In the RA group, more than half (56.7%) had problems with the TMJ, 70% of them had masseter hypertrophy and clicks in the TMJ, and 46.7% had tinnitus (in the control group: 10%, 30%, and 30%, respectively). Patients also had a limited range of abduction movement in the TMJ (38.0 ±6.1 mm). Analysis of the pain map of Prof. Mariano Rocabado in RA patients indicates a sig

nificantly greater number of pain structures. In the control group no pain was observed in structures such as the posterosuperior synovial and bilaminar zone, posterior ligament, or retrodiscal area.

Conclusions: Temporomandibular joint problems in RA patients were more serious than in the con

trol group and these differences were statistically significant for most tests. The awareness of the problem with the TMJ in RA patients is very low; participants of our study were 100% unaware that the function of the TMJ could be improved. Additionally, there are no guidelines for the treatment and rehabilitation of these joints.

Key words: pain, rheumatoid arthritis, temporomandibular joint, temporomandibular disorders.

Introduction

Temporomandibular disorders (TMD) are common reasons for visiting a specialist. Reports from the Natio

nal Institute of Dental and Craniofacial Research indi

cate that the problems associated with this joint are the second most frequent complaints reported immediately after back pain [1]. They may affect as many as 5–12% of the whole population, which generates enormous costs associated with the treatment [1].

Every fifth person may have a problem with the temporomandibular joint (TMJ) of various etiologies [2].

Temporomandibular disorders cover, in a very broad sense, problems of patients in the orofacial region. Most often pain is related to dysfunction of the periarticular structures, as well as to disorders affecting the joint itself [3].

Rheumatoid arthritis (RA) is an immunemediated inflammatory disease. Most often, the illness initially

Address for correspondence:

Beata Sokołowska, Bioinformatics Laboratory, Mossakowski Medical Research Centre, Polish Academy of Sciences, 5 Pawińskiego St., 02106 Warsaw, Poland, email: beta.sokolowska@imdik.pan.pl

Submitted: 11.05.2020; Accepted: 25.06.2021

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affects the small joints of the hands and feet. The dis

ease affects symmetrical joints in which we observe swelling, warming and limitation of their function. Pain is a constant symptom [4].

Only very few studies pay attention to TMJ problems in patients with RA. In diagnostics of RA patients, deter

mination of the inflammatory changes in the synovium of these joints occurred in 100% of patients, while in the control group it was only 2%, which provides direct con

firmation of the relationship between the disease and the joint [5].

Imaging studies such as magnetic resonance (MR) and cone beam computed tomography (CBCT) of the TMJ indicate narrowing of the joint disc and its perfo

ration, and also a tendency to more frequent erosive changes, subchondral sclerotization and flattening of the mandible bone head [6, 7].

The study aims to draw the attention of patients, doctors and therapists to the importance of TMJ prob

lems in patients with RA.

Material and methods

Patients

The research was conducted at the National Institute of Geriatric Rheumatology and Rehabilitation (NIGRR) in Warsaw. It involved 60 subjects in two groups. The first group consisted of 30 patients: 23 (76.7%) women and 7 (23.3%) men with diagnosed RA.

The inclusion criteria were as follows: diagnosed RA according to the American College of Rheumatology (ACR)/European League Against Rheumatism (EULAR) criteria [8] and age in the range of 18–65 years, while we excluded from the group people who had a history of craniofacial trauma or orofacial surgery.

The second, control group (30 subjects) consisted of healthy volunteers at a comparable age to subjects in the RA group, 18 (60%) women and 12 men (40%). The average age for the RA group was 49.1 ±13.0 (median 50), and for the control group 49.0 ±8.5 (median 48) years.

The research project was approved by the Bioethics Committee of NIGRR (approval number KBT8/9/2018), and all methods were carried out in accordance with relevant guidelines and regulations. All subjects/partic

ipants gave written informed consent for participation in the study.

Methods

To obtain general information about the age, dura

tion of the disease and issues related to the subjective assessment of problems in the TMJ and possible therapy in this area, teeth clenching, as well as the occurrence of

clicking in the TMJs and tinnitus, the relevant personal questionnaires were used.

The study used the Visual Analogue Scale (VAS) for subjective assessment of the level of pain in the exa

mined joints. The subject examination consisted of assessing the symmetry of the head and occlusion.

The study began with an evaluation of the symmetry of the occlusion as well as the quality of the lower jaw movements in the sitting position, without correction.

The position of the head in space in the sagittal and frontal plane in relation to the entire trunk was as

sessed. Face contour was analyzed to assess the level of masseter muscle development. In the supine position, the patients were asked to perform maximal mandible abduction (mouth opening); the measurement was per

formed twice with a disposable wooden spatula and the more accurate results were recorded in millimeters.

Temporomandibular joints were also palpated. The test was considered positive when it caused pain. The asses

sment of 8 structures was made according to the joint pain map of Prof. Mariano Rocabado, as follows: 1 – ante

roinferior synovial, 2 – anterosuperior synovial, 3 – late

ral collateral ligament, 4 – temporomandibular liga

ment, 5 – posteroinferior synovial, 6 – posterosuperior synovial, 7 – bilaminar zone or posterior ligament and 8 – retrodiscal area [9–11].

Statistical analysis

For the statistical analyses we used the STATISTICA software version 9.0 (StatSoft Inc.). Qualitative data were expressed as a count and percentages, and for the con

tingency tables the χ²test was used, taking into account relevant corrections for this test. Quantitative data were presented as mean and standard deviation (SD), median, and range of minimum and maximum.

Due to the nonGaussian distribution of the analyzed variables, the nonparametric MannWhitney U test was used to analyze differences between the studied groups or various research conditions. In the correlation anal

ysis, Spearman’s rank correlation coefficient (ρ) values were calculated. Probability values were considered sta

tistically significant for p < 0.05.

Results

Table I shows the results of the VAS pain scale anal

ysis in both groups. In the RA group at rest, half of the participants (n = 15) experienced pain at an average lev

el of 3.7 ±2.5 (median 3.0), and in the control group no pain at rest was observed.

During the activities (such as yawning, eating or other movements) 18 subjects (60%) of the RA group re

ported pain, the VAS increased to 5.7 ±2.4 (median 6.2),

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but only 4 people (13.3%) experienced pain in the control group (3.4 ±3.0, median 2.5). The observed population differences between two study groups are significant, p = 0.00001 and p = 0002, respectively.

In the RA group, the calculated Disease Activity Score 28 (DAS28) was equal to 5.4 ±1.5 (median 5.6), which corresponds to high disease activity. It is also re

flected in the levels of inflammatory parameters such as ery throcyte sedimentation rate (ESR) and Creactive protein (CRP) serum concentration, i.e. 34.0 ±19.3 mm/h (median 34) and 19.6 ±15.7 mg/l (median 15).

The results of the completed questionnaires are presented in Table II. They indicate that in the RA group more than half of the respondents (56.7%) had prob

lems in the TMJs, while in the control group only 3 sub

jects did so (10%) (p = 0.00013). None of the participants in either group was treated for TMD.

In the case of tooth clenching symptoms, in the RA group 63.3% of patients clench their teeth, while in the

control group this symptom occurs in 36.7% (p = 0.039).

In turn, assessing facial symmetry in relation to the ru

men muscle superstructure, muscle hypertrophy was ob

served in 70% of the RA patients and 30% of the healthy controls (p = 0.002).

Table III shows the results regarding the occurrence of acoustic phenomena (clicks) in the TMJ and tinnitus in the examined groups. In the RA group, clicks in the right temporomandibular joint (rTMJ) were observed in 60% of patients, and in the left temporomandibular joint (lTMJ) in 43.3%, and clicking averages were 4.8 ±2.5 (median 4.6) for the rTMJ and 5.4 ±1.9 (median 4.9) for the lTMJ. In the control group only 7 subjects (23.3%) re

ported clicking in the rTMJ, and in the lTMJ slightly more, 9 subjects (30%). The number of clicks was lower: for the rTMJ about 3.6 ±1.9 (median 3.0) and for the lTMJ about 3.2 ±1.7 (median 2.0).

In patients with RA, tinnitus occurred in the right ear in 43.3% at the level of 4.6 ±2.4 (median 4.0), and in the Table I. Results for the Visual Analogue Scale

Parameter of VAS RA Control Test p-value

At rest

VAS = 0, n (%) 15 (50) 30 (100) χ² test (correction of V²) 0.00001

VAS > 0, n (%) 15 (50) 0 (0)

Mean ±SD 3.7 ±2.5

Median 3.0

(Min; Max) (0.2; 7.4)

During activity

VAS = 0, n (%) 12 (40) 26 (86.7) χ² test

U^M-W test

0.0002 0.166

VAS > 0, n (%) 18 (60) 4 (13.3)

Mean ±SD 5.7 ±2.4 3.4 ±3.0

Median 6.2 2.5

(Min; Max) (0.2; 9.0) (0.8; 7.6)

RA – rheumatoid arthritis, VAS – Visual Analogue Scale.

Table II. Answers to the questionnaires

Questionnaires RA [n (%)] Control [n (%)] Test p-value

TMJ problems

Yes 17 (56.7) 3 (10) χ² test 0.0001

No 13 (43.3) 27 (90)

Teeth clenching

Yes 19 (63.3) 11 (36.7) χ² test 0.039

No 11 (36.7) 19 (63.3)

Expanded masseters

Yes 21 (70) 9 (30) χ² test 0.002

No 9 (30) 21 (70)

RA – rheumatoid arthritis, TMJ – temporomandibular joint.

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Table III. Results of acoustic phenomena (clicks) in the temporomandibular joint and tinnitus

Signs RA Control Test p-value

Clicks in the right TMJ

No, n (%) 12 (40) 23 (76.7) χ² test 0.004

Yes, n (%) 18 (60) 7 (23.3)

Clicks

Mean ±SD 4.8 ±2.5 3.6 ±1.9 U^M-W test 0.297

Median 4.6 3.0

(Min; Max) (0.9; 10.0) (1.9; 7.0)

Clicks in the left TMJ

No, n (%) 17 (56.7) 21 (70) χ² test 0.284

Yes, n (%) 13 (43.3) 9 (30)

Clicks

Mean ±SD 5.4 ±1.9 3.2 ±1.7 U^M-W test 0.009

Median 4.9 2.0

(Min; Max) (2.7; 8.1) (1.9; 7.0)

Summary of clicks in TMJ

No, n (%) 9 (30) 19 (63.3) χ² test 0.010

Yes, n (%) 21 (70) 11 (36.7)

Clicks

Mean ±SD 4.9 ±2.4 3.4 ±1.6 U^M-W test 0.074

Median 4.6 3.0

(Min; Max) (0.9; 10.0) (1.9; 7.0)

Tinnitus in the right ear

No, n (%) 17 (56.7) 22 (73.3) χ² test 0.176

Yes, n (%) 13 (43.3) 8 (26.7)

Tinnitus

Mean ±SD 4.6 ±2.4 2.9 ±2.7 U^M-W test 0.089

Median 4.0 2.0

(Min; Max) (1.4; 9.0) (0.3; 8.0)

Tinnitus in the left ear

No, n (%) 19 (63.3) 22 (73.3) χ² test 0.405

Yes, n (%) 11 (36.7) 8 (26.7)

Tinnitus

Mean ±SD 5.2 ±2.5 2.5 ±2.4 U^M-W test 0.020

Median 4.8 2.0

(Min; Max) (1.4; 9.0) (0.3; 8.0)

Summary of tinnitus

No, n (%) 16 (53.3) 21 (70) χ² test 0.184

Yes, n (%) 14 (46.7) 9 (30)

Tinnitus

Mean ±SD 4.8 ±2.4 2.9 ±2.6 U^M-W test 0.063

Median 4.4 2.0

(Min; Max) (1.4; 9.0) (0.3; 8.0)

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left ear in 36.7% at the level of 5.2 ±2.5 (median 4.8).

In general, there were no clicks in the TMJ in 30% of RA patients and 63.3% of healthy controls (p = 0.010), and no tinnitus in 53.3% of the RA group and in 70% of the control group (p = 0.184).

The mean level of clicks in RA patients was higher than in healthy participants (i.e. 4.9 ±2.4 and median 4.6 vs. 3.4 ±1.6 and median 3.0, p = 0.074). The mean number of cases of tinnitus in the RA was also higher than in the control group (i.e. 4.8 ±2.4 and median 4.4 vs.

2.9 ±2.6 and median 2.0, p = 0.063).

Analysis of the limited range of abduction motion in the TMJ (Table IV) indicates that in the RA group the range is significantly lower (mean 38.0 ±6.1 mm and me

dian 39.3) than in the control group (mean 45.9 ±5.3 mm and median 46.3) (p = 0.000001).

It was observed that only 46.7% of patients with RA achieved the range above the abduction norm (i.e. 42.7

±2.9 mm, median 41.8). In the control group, only 4 sub

jects (13.3%) did not reach the norm. The observed dif

ferences between the examined groups are significant (Table IV).

Results of the occurrence of painful structures accord

ing to the joint pain map of Prof. Rocabado are presented in Tables V–VI. As shown in Table V, RA patients have about half as many painless areas as healthy controls, and painsensitive structures are more common (the differences between groups are statistically significant, p = 0.006). None of the studied subjects reported sensi

tivity at once in all pain areas of Prof. Rocabado’s map.

The results presented in Table VI, which take into account the frequency of individual painful structures according to the joint pain map of Prof. Rocabado, in

dicate that structures numbered 1–5 are painful in both examined groups, while in the RA group they are affect

ed more often than in the control. There was no pain in structures 6–8 in healthy individuals, and among them, structure 6, i.e. the posterosuperior synovial zone, may be of particular importance.

Moreover, in the RA group significant strong positive correlations of TMJ pain and inflammatory parameters of ESR and CRP were observed; correlation coefficient values are ρ = 0.71 (p = 0.0002) and ρ = 0.56 (p = 0.007), respectively. Significant correlations were also observed Table IV. Results for abduction movement of the temporomandibular joint

Abduction movement RA Control Test p-value

Motion range (mm)

Mean ±SD 38.0 ±6.1 45.9 ±5.3 U^M-W test 0.000001

Median 39.3 46.3

(Min; Max) (22.0; 49.0) (33.5; 60.0)

Below the norm (< 40 mm)

Number (%) 16 (53.3) 4 (13.3) (Below vs. above the norm)

Mean ±SD 33.8 ±5.1 37.6 ±2.8

Median 34.8 38.8

(Min; Max) (22.0; 39.5) (33.5; 39.5)

Above the norm

Number (%) 14 (46.7) 26 (86.7) χ² test

U^M-W test

0.001 0.0005

Mean ±SD 42.7 ±2.9 47.2 ±4.3

Median 41.8 46.8

(Min; Max) (40.0; 49.0) (41.0; 60.0)

RA – rheumatoid arthritis.

Table V. General distribution of pain-sensitive structures in the temporomandibular joint Pain-sensitive

structures RA, n Control, n

Right TMJ Left TMJ Total Right TMJ Left TMJ Total

None 8 10 18 18 15 33

Whichever 22 20 42 12 15 27

All 0 0 0 0 0 0

χ² test p = 0.006

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Table VI. Distribution of sensitive structures according to the joint pain map of Prof. Mariano Rocabado

Name of structure RA, n Control, n

Right TMJ Left TMJ Total Right TMJ Left TMJ Total

1 – Anteroinferior synovial 17 14 31 5 5 10

2 – Anterosuperior synovial 15 13 28 4 4 8

3 – Lateral collateral ligament 16 15 31 6 6 12

4 – Temporomandibular ligament 21 17 38 8 10 18

5 – Posteroinferior synovial 21 17 38 8 10 18

6 – Posterosuperior synovial 19 17 36 0 0 0

7 – Bilaminar zone 3 3 6 0 0 0

8 – Retrodiscal area 1 0 1 0 0 0

Sum 113 96 209 31 35 66

between the parameters of pain assessment in the joint and the abduction movement with the disease duration, i.e. the positive correlation ρ = 0.41 (p = 0.024) and the negative correlation ρ = –0.36 (p = 0.048), respectively.

Discussion

According to the current literature, RA affects the TMJ, although the conclusions are not consistent. That may result from different research methods, diverse se

lection of groups and a range of their counts [12–18].

Shoohanizad et al. [19] stated that TMD occurs in auto immune diseases such as RA, systemic sclerosis and lupus erythematosus. The analysis of articles se

lected by the authors indicates that the early diagno

sis of problems in the TMJs slows down the progression of degenerative changes in these joints. That leads to a reduction of treatment costs. Therefore, it is recom

mended to conduct research on the TMD problem in relationship with connective tissue illnesses resulting from autoimmune diseases.

Our study involved 60 people, divided into two groups: patients with RA (n = 30) and healthy controls (n = 30). In the RA group 17 patients (57%) report

ed TMD, while only 3 (10%) healthy individuals did so (p = 0.0001).

Lin et al. [20] examined a group of 17,317 patients with rheumatoid arthritis along with an equal number of controls and they found that in the RA group TMD was 2.5 times more frequent (p < 0.001). There was also a significant correlation of TMD in females, subjects with mental problems as well as patients after a stroke episode (p < 0.001). A few studies have reported the re

lationship between RA and the occurrence of TMJ symp

toms [20–23]. It mainly manifests in the occurrence of pain, limitation of mandible movements, as well as

auditory phenomena and palpation sensitivity of the joint [20–22].

A significant difference in functional mandible move

ment (p = 0.000001) was observed in the present study, similar to the work of Mortazavi et al. [24]. In the cited work the authors also obtained a significant result in RA patients for the occurrence of auditory phenomena (p < 0.01) for left and right joints.

In the study by Lin et al. [16], people with RA were also examined for TMD. They found that 13 (23%) patients did not reach the abduction norm (40 mm); in our study as many as 60% of patients (18 cases out of 30) did so.

The average range of abduction in YiChun Lin’s study was 42.2 ±0.8 mm, while in ours it was 38.0 ±6.1 mm.

Gleissner et al. [25] also observed that the RA patients achieved a lower average abduction (40.6

±6.5 mm) compared to healthy subjects with an aver

age of 45.8 ±5.5 mm (p < 0.001). They obtained similar results to those described in our study for the control group, i.e. 45.9 ±5.3 mm.

Alstergren et al. [26] concluded that patients with RA have a significant reduction in mandibular movement (full abduction, p < 0.001).

Dev et al. [27] observed a significant reduction in the abduction movement among RA patients (p < 0.05); this study was conducted on older RA patients over 60 years old. The results of our study are corroborated by those of Dev et al. [27].

Regarding the level of sensitivity during rest and jaw movement, Ahmed et al. [28] found frequent occurrence of pain in the TMJ in RA patients; only 3 out of 33 (9%) reported no complaints concerning the TMJ, while in our study 15 (50%) subjects reported pain at rest and 18 (60%) during activity (statistically significant differ

ences compared to the control group, p = 0.0002).

Crincoli et al. [29] noted that fewer RA patients com

plained about chewing pain, tinnitus and difficulty in

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opening the mouth than in the control group, which is not confirmed by our results.

In the study of Witulski et al. [6] 30% of patients reported complaints in the TMJ area, 63% of the neck, 73% of the upper limb girdle, while only 7% out of the control group had TMJ pain. In the cited study 70% of RA patients suffered from pain during jaw movements, and 40% of patients had clicks in their joints, whereas none of the healthy people reported such complaints.

Our results confirmed the presence of TMD in RA patients. 21 patients (70%) affirmed the occurrence of clicking in the joint, compared to only 11 (36.7%) in the control group. 18 subjects (60%) reported mandible dis

comfort, and only 4 (13.3%) in the healthy group.

Analyzing in the anamnesis and the physical exam in 40 patients Bracco et al. [30] found that 19 of them (47.5%) presented pain symptoms from the posterior TMJ, which is slightly lower than the number in our study, where 21 (70%) people with RA in the right joint and 17 (56.7%) in the left reported pain in this structure. Pal

pation of structures such as the posterosuperior synovial and bilaminar zone, posterior ligament, and retro discal area, according to the joint pain map of Prof. Rocabado [9, 10], may be crucial in differentiating between the pa

tients and control groups because none of the healthy subjects had experienced pain in this area.

The main limi tation of this study is the small size of the studied groups. Therefore these study can be con sidered preliminary. Further observation of the de

scribed patients and analysis of TMD cases in RA will allow to better docu ment the problem and work out the methods of managements.

Conclusions

The TMJ problems in RA patients are more serious than in the control group and for most tests the differ

ences were significant. The relationship between RA and TMD is confirmed in the literature. However, there is no standardized evaluation protocol that could unify the conducted research.

The awareness of the problem with the TMJ in RA pa

tients is very low. All subjects who participated in the pres

ent study were unaware that the function of the TMJ could be improved. Additionally, there are no uniform guidelines for the treatment and rehabilitation of these joints.

The authors declare no conflict of interest.

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